Dopamine and Cognitive Control in Prefrontal Cortex

Cognitive control, the ability to orchestrate behavior in accord with our goals, depends on the prefrontal cortex. These cognitive functions are heavily influenced by the neuromodulator dopamine. We review here recent insights exploring the influence of dopamine on neuronal response properties in prefrontal cortex (PFC) during ongoing behaviors in primates. This review suggests three major computational roles of dopamine in cognitive control: (i) gating sensory input, (ii) maintaining and manipulating working memory contents, and (iii) relaying motor commands. For each of these roles, we propose a neuronal microcircuit based on known mechanisms of action of dopamine in PFC, which are corroborated by computational network models. This conceptual approach accounts for the various roles of dopamine in prefrontal executive functioning.

[1]  Steven P. Wise,et al.  Forward frontal fields: phylogeny and fundamental function , 2008, Trends in Neurosciences.

[2]  K. Harris,et al.  Cortical connectivity and sensory coding , 2013, Nature.

[3]  Minryung R. Song,et al.  Multiphasic Temporal Dynamics in Responses of Midbrain Dopamine Neurons to Appetitive and Aversive Stimuli , 2013, The Journal of Neuroscience.

[4]  A. Björklund,et al.  Dopamine neuron systems in the brain: an update , 2007, Trends in Neurosciences.

[5]  J. Berke.  What does dopamine mean? , 2018, Nature Neuroscience.

[6]  R. O’Reilly,et al.  A computational approach to prefrontal cortex, cognitive control and schizophrenia: recent developments and current challenges. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[7]  Markus Siegel,et al.  Cortical information flow during flexible sensorimotor decisions , 2015, Science.

[8]  R. Romo,et al.  Neuronal correlates of subjective sensory experience , 2005, Nature Neuroscience.

[9]  P. Goldman-Rakic,et al.  The role of D1-dopamine receptor in working memory: local injections of dopamine antagonists into the prefrontal cortex of rhesus monkeys performing an oculomotor delayed-response task. , 1994, Journal of neurophysiology.

[10]  N. Uchida,et al.  Dopamine neurons projecting to the posterior striatum reinforce avoidance of threatening stimuli , 2018, Nature Neuroscience.

[11]  Stephanie Westendorff,et al.  Dopamine Receptors Influence Internally Generated Oscillations during Rule Processing in Primate Prefrontal Cortex , 2018, Journal of Cognitive Neuroscience.

[12]  Matthew T. Kaufman,et al.  An optogenetic toolbox designed for primates , 2011, Nature Neuroscience.

[13]  Andreas Nieder,et al.  Numerical Rule Coding in the Prefrontal, Premotor, and Posterior Parietal Cortices of Macaques , 2012, The Journal of Neuroscience.

[14]  W. Schultz.  Behavioral theories and the neurophysiology of reward. , 2006, Annual review of psychology.

[15]  Susana Q. Lima,et al.  Complementary Contributions of Striatal Projection Pathways to Action Initiation and Execution , 2016, Cell.

[16]  P. Goldman-Rakic,et al.  Dopamine Modulation of Perisomatic and Peridendritic Inhibition in Prefrontal Cortex , 2003, The Journal of Neuroscience.

[17]  M. Ragozzino,et al.  The effects of dopamine D(1) receptor blockade in the prelimbic-infralimbic areas on behavioral flexibility. , 2002, Learning & memory.

[18]  Ilana B. Witten,et al.  Reward and choice encoding in terminals of midbrain dopamine neurons depends on striatal target , 2016, Nature Neuroscience.

[19]  G. Lubec,et al.  Spatial Working Memory in Male Rats: Pre-Experience and Task Dependent Roles of Dopamine D1- and D2-Like Receptors , 2017, Front. Behav. Neurosci..

[20]  A. Arnsten,et al.  Neuromodulation of Thought: Flexibilities and Vulnerabilities in Prefrontal Cortical Network Synapses , 2012, Neuron.

[21]  Jonathan D. Cohen,et al.  Computational perspectives on dopamine function in prefrontal cortex , 2002, Current Opinion in Neurobiology.

[22]  David J. Freedman,et al.  Representation of the Quantity of Visual Items in the Primate Prefrontal Cortex , 2002, Science.

[23]  D. Durstewitz,et al.  The ability of the mesocortical dopamine system to operate in distinct temporal modes , 2007, Psychopharmacology.

[24]  Carrie J. McAdams,et al.  Effects of Attention on the Reliability of Individual Neurons in Monkey Visual Cortex , 1999, Neuron.

[25]  Masayuki Matsumoto,et al.  Distinct Representations of Cognitive and Motivational Signals in Midbrain Dopamine Neurons , 2013, Neuron.

[26]  Josiah R. Boivin,et al.  A Causal Link Between Prediction Errors, Dopamine Neurons and Learning , 2013, Nature Neuroscience.

[27]  D. Durstewitz,et al.  The Dual-State Theory of Prefrontal Cortex Dopamine Function with Relevance to Catechol-O-Methyltransferase Genotypes and Schizophrenia , 2008, Biological Psychiatry.

[28]  E. Miller,et al.  Task-specific neural activity in the primate prefrontal cortex. , 2000, Journal of neurophysiology.

[29]  F. Artigas,et al.  Laminar and Cellular Distribution of Monoamine Receptors in Rat Medial Prefrontal Cortex , 2017, Front. Neuroanat..

[30]  P. Goldman-Rakic,et al.  Dopamine D1 receptor mechanisms in the cognitive performance of young adult and aged monkeys , 1994, Psychopharmacology.

[31]  Jude F. Mitchell,et al.  Differential Attention-Dependent Response Modulation across Cell Classes in Macaque Visual Area V4 , 2007, Neuron.

[32]  J. Horvitz.  Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events , 2000, Neuroscience.

[33]  G. E. Alexander,et al.  Neuron Activity Related to Short-Term Memory , 1971, Science.

[34]  T. Moore,et al.  CONTROL OF VISUAL CORTICAL SIGNALS BY PREFRONTAL DOPAMINE , 2011, Nature.

[35]  S. Wise,et al.  Rule-dependent neuronal activity in the prefrontal cortex , 1999, Experimental Brain Research.

[36]  S. McGurk,et al.  Schizophrenia , 2004, The Lancet.

[37]  Zhen Yan,et al.  Distinct Physiological Effects of Dopamine D4 Receptors on Prefrontal Cortical Pyramidal Neurons and Fast-Spiking Interneurons. , 2016, Cerebral cortex.

[38]  J. Mayhew,et al.  How Visual Stimuli Activate Dopaminergic Neurons at Short Latency , 2005, Science.

[39]  M. Petrides.  Lateral prefrontal cortex: architectonic and functional organization , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[40]  Naoshige Uchida,et al.  Arithmetic and local circuitry underlying dopamine prediction errors , 2015, Nature.

[41]  P S Goldman-Rakic,et al.  Widespread origin of the primate mesofrontal dopamine system. , 1998, Cerebral cortex.

[42]  Ethan S. Bromberg-Martin,et al.  Dopamine in Motivational Control: Rewarding, Aversive, and Alerting , 2010, Neuron.

[43]  P. Goldman-Rakic,et al.  Heterogeneous targets of dopamine synapses in monkey prefrontal cortex demonstrated by serial section electron microscopy: a laminar analysis using the silver-enhanced diaminobenzidine sulfide (SEDS) immunolabeling technique. , 1993, Cerebral cortex.

[44]  A. Nieder.  The neuronal code for number , 2016, Nature Reviews Neuroscience.

[45]  K. Deisseroth,et al.  Input-specific control of reward and aversion in the ventral tegmental area , 2012, Nature.

[46]  P. Goldman-Rakic,et al.  Selective D2 Receptor Actions on the Functional Circuitry of Working Memory , 2004, Science.

[47]  T. Robbins,et al.  Systemic sulpiride in young adult volunteers simulates the profile of cognitive deficits in Parkinson’s disease , 1999, Psychopharmacology.

[48]  Hidehiko Takahashi,et al.  Functional significance of central D1 receptors in cognition: beyond working memory , 2012, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[49]  A. Nieder,et al.  Complementary Contributions of Prefrontal Neuron Classes in Abstract Numerical Categorization , 2008, The Journal of Neuroscience.

[50]  Tatiana Pasternak,et al.  Flexibility of Sensory Representations in Prefrontal Cortex Depends on Cell Type , 2009, Neuron.

[51]  Andreas Nieder,et al.  Compressed Scaling of Abstract Numerosity Representations in Adult Humans and Monkeys , 2009, Journal of Cognitive Neuroscience.

[52]  Andreas Nieder,et al.  Representation of Abstract Quantitative Rules Applied to Spatial and Numerical Magnitudes in Primate Prefrontal Cortex , 2013, The Journal of Neuroscience.

[53]  M. Howe,et al.  Rapid signaling in distinct dopaminergic axons during locomotion and reward , 2016, Nature.

[54]  Roshan Cools,et al.  The cost of dopamine for dynamic cognitive control , 2015, Current Opinion in Behavioral Sciences.

[55]  J. Cohen,et al.  Dopamine, cognitive control, and schizophrenia: the gating model. , 1999, Progress in brain research.

[56]  S C Rao,et al.  Integration of what and where in the primate prefrontal cortex. , 1997, Science.

[57]  Tirin Moore,et al.  Dissociable dopaminergic control of saccadic target selection and its implications for reward modulation , 2013, Proceedings of the National Academy of Sciences.

[58]  Daniel Durstewitz,et al.  The computational role of dopamine D1 receptors in working memory , 2002, Neural Networks.

[59]  Fumitoshi Kodaka,et al.  Differential Contributions of Prefrontal and Hippocampal Dopamine D1 and D2 Receptors in Human Cognitive Functions , 2008, The Journal of Neuroscience.

[60]  T. Sawaguchi,et al.  The effects of dopamine and its antagonists on directional delay-period activity of prefrontal neurons in monkeys during an oculomotor delayed-response task , 2001, Neuroscience Research.

[61]  Andreas Nieder,et al.  Complementary Roles for Primate Frontal and Parietal Cortex in Guarding Working Memory from Distractor Stimuli , 2014, Neuron.

[62]  Philip Seeman,et al.  Atypical Antipsychotics: Mechanism of Action , 2002, Canadian journal of psychiatry. Revue canadienne de psychiatrie.

[63]  Tatiana Pasternak,et al.  Memory-Guided Sensory Comparisons in the Prefrontal Cortex: Contribution of Putative Pyramidal Cells and Interneurons , 2012, The Journal of Neuroscience.

[64]  W. Schultz.  Predictive reward signal of dopamine neurons. , 1998, Journal of neurophysiology.

[65]  X. Wang,et al.  Synaptic Basis of Cortical Persistent Activity: the Importance of NMDA Receptors to Working Memory , 1999, The Journal of Neuroscience.

[66]  D. M. Jackson,et al.  Dopamine receptors: molecular biology, biochemistry and behavioural aspects. , 1994, Pharmacology & therapeutics.

[67]  S. Floresco,et al.  Multiple Dopamine Receptor Subtypes in the Medial Prefrontal Cortex of the Rat Regulate Set-Shifting , 2006, Neuropsychopharmacology.

[68]  S. Everling,et al.  Dopamine D1 and D2 Receptors Make Dissociable Contributions to Dorsolateral Prefrontal Cortical Regulation of Rule-Guided Oculomotor Behavior. , 2016, Cell reports.

[69]  P. Dayan,et al.  A framework for mesencephalic dopamine systems based on predictive Hebbian learning , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[70]  Andreas Nieder,et al.  Neuronal Correlates of Visual Working Memory in the Corvid Endbrain , 2014, The Journal of Neuroscience.

[71]  T. Braver,et al.  Dopamine Does Double Duty in Motivating Cognitive Effort , 2016, Neuron.

[72]  William R. Stauffer,et al.  Dopamine neurons learn relative chosen value from probabilistic rewards , 2016, eLife.

[73]  K. Deisseroth,et al.  Striatal Dopamine Release Is Triggered by Synchronized Activity in Cholinergic Interneurons , 2012, Neuron.

[74]  S. Everling,et al.  Neuromodulation of Prefrontal Cortex in Non-Human Primates by Dopaminergic Receptors during Rule-Guided Flexible Behavior and Cognitive Control , 2017, Front. Neural Circuits.

[75]  Tatiana Pasternak,et al.  Common Rules Guide Comparisons of Speed and Direction of Motion in the Dorsolateral Prefrontal Cortex , 2013, The Journal of Neuroscience.

[76]  D. Durstewitz,et al.  Bidirectional Dopamine Modulation of GABAergic Inhibition in Prefrontal Cortical Pyramidal Neurons , 2001, The Journal of Neuroscience.

[77]  William Bialek,et al.  Adaptive Rescaling Maximizes Information Transmission , 2000, Neuron.

[78]  R. Romo,et al.  Dopamine neurons code subjective sensory experience and uncertainty of perceptual decisions , 2011, Proceedings of the National Academy of Sciences.

[79]  A. Thiele,et al.  Neuromodulation of Attention , 2018, Neuron.

[80]  M. D’Esposito,et al.  Individual capacity differences predict working memory performance and prefrontal activity following dopamine receptor stimulation , 2005, Cognitive, affective & behavioral neuroscience.

[81]  Andreas Nieder,et al.  Basic mathematical rules are encoded by primate prefrontal cortex neurons , 2010, Proceedings of the National Academy of Sciences.

[82]  Earl K. Miller,et al.  Laminar recordings in frontal cortex suggest distinct layers for maintenance and control of working memory , 2018, Proceedings of the National Academy of Sciences.

[83]  N. Uchida,et al.  Neural Circuitry of Reward Prediction Error. , 2017, Annual review of neuroscience.

[84]  W. Schultz,et al.  Coding of Predicted Reward Omission by Dopamine Neurons in a Conditioned Inhibition Paradigm , 2003, The Journal of Neuroscience.

[85]  T. Klingberg,et al.  Prefrontal cortex and basal ganglia control access to working memory , 2008, Nature Neuroscience.

[86]  P. Goldman-Rakic,et al.  Intrinsic circuit organization of the major layers and sublayers of the dorsolateral prefrontal cortex in the rhesus monkey , 1995, The Journal of comparative neurology.

[87]  S. Funahashi,et al.  Population vector analysis of primate prefrontal activity during spatial working memory. , 2004, Cerebral cortex.

[88]  Andreas Nieder,et al.  A Labeled-Line Code for Small and Large Numerosities in the Monkey Prefrontal Cortex , 2007, The Journal of Neuroscience.

[89]  W. Schultz,et al.  Responses of monkey midbrain dopamine neurons during delayed alternation performance , 1991, Brain Research.

[90]  G. Mengod,et al.  D2 and D4 dopamine receptor mRNA distribution in pyramidal neurons and GABAergic subpopulations in monkey prefrontal cortex: implications for schizophrenia treatment , 2010, Neuroscience.

[91]  Arthur P. Shimamura,et al.  The role of the prefrontal cortex in dynamic filtering , 2000, Psychobiology.

[92]  C. Lay,et al.  Differential contributions of dopaminergic D1- and D2-like receptors to cognitive function in rhesus monkeys , 2006, Psychopharmacology.

[93]  Jerald D. Kralik,et al.  Representation of Attended Versus Remembered Locations in Prefrontal Cortex , 2004, PLoS biology.

[94]  A. Nieder,et al.  Dopamine Regulates Two Classes of Primate Prefrontal Neurons That Represent Sensory Signals , 2013, The Journal of Neuroscience.

[95]  J. Duncan,et al.  Filtering of neural signals by focused attention in the monkey prefrontal cortex , 2002, Nature Neuroscience.

[96]  W. Schultz,et al.  Responses of monkey dopamine neurons during learning of behavioral reactions. , 1992, Journal of neurophysiology.

[97]  M. Poo,et al.  Phasic dopamine release in the medial prefrontal cortex enhances stimulus discrimination , 2016, Proceedings of the National Academy of Sciences.

[98]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

[99]  T. Sejnowski,et al.  Dopamine-mediated stabilization of delay-period activity in a network model of prefrontal cortex. , 2000, Journal of neurophysiology.

[100]  S. Floresco,et al.  Mesocortical dopamine modulation of executive functions: beyond working memory , 2006, Psychopharmacology.

[101]  J D Cohen,et al.  A network model of catecholamine effects: gain, signal-to-noise ratio, and behavior. , 1990, Science.

[102]  C. Fiebach,et al.  Dissociable fronto-striatal effects of dopamine D2 receptor stimulation on cognitive versus motor flexibility , 2013, Cortex.

[103]  E. K. Miller,et al.  Executive Function and Higher-Order Cognition: Definition and Neural Substrates , 2008 .

[104]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[105]  P. Goldman-Rakic,et al.  Regional, cellular, and subcellular variations in the distribution of D1 and D5 dopamine receptors in primate brain , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[106]  P S Goldman-Rakic,et al.  Layer V neurons bear the majority of mRNAs encoding the five distinct dopamine receptor subtypes in the primate prefrontal cortex , 1998, Synapse.

[107]  J. Zylberberg,et al.  Mechanisms of Persistent Activity in Cortical Circuits: Possible Neural Substrates for Working Memory. , 2017, Annual review of neuroscience.

[108]  W. Newsome,et al.  Context-dependent computation by recurrent dynamics in prefrontal cortex , 2013, Nature.

[109]  Christos Constantinidis,et al.  The sensory nature of mnemonic representation in the primate prefrontal cortex , 2001, Nature Neuroscience.

[110]  German Barrionuevo,et al.  Selective reduction by dopamine of excitatory synaptic inputs to pyramidal neurons in primate prefrontal cortex , 2002, The Journal of physiology.

[111]  Xiao-Jing Wang,et al.  Erratum to: Effects of neuromodulation in a cortical network model of object working memory dominated by recurrent inhibition , 2014, Journal of Computational Neuroscience.

[112]  P. Goldman-Rakic,et al.  Subcellular localization of the dopamine D2 receptor and coexistence with the calcium‐binding protein neuronal calcium sensor‐1 in the primate prefrontal cortex , 2005, The Journal of comparative neurology.

[113]  P. Goldman-Rakic,et al.  Presynaptic regulation of recurrent excitation by D1 receptors in prefrontal circuits. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[114]  P. Goldman-Rakic,et al.  D1 receptors in prefrontal cells and circuits , 2000, Brain Research Reviews.

[115]  Luigi F. Agnati,et al.  The emergence of the volume transmission concept 1 Published on the World Wide Web on 12 January 1998. 1 , 1998, Brain Research Reviews.

[116]  Jonathan D. Cohen,et al.  Role of prefrontal cortex and the midbrain dopamine system in working memory updating , 2012, Proceedings of the National Academy of Sciences.

[117]  W. Schultz,et al.  Dopamine neurons of the monkey midbrain: contingencies of responses to stimuli eliciting immediate behavioral reactions. , 1990, Journal of neurophysiology.

[118]  A. Arnsten,et al.  Neurobiology of Executive Functions: Catecholamine Influences on Prefrontal Cortical Functions , 2004, Biological Psychiatry.

[119]  Torben Ott,et al.  Dopamine Receptors Differentially Enhance Rule Coding in Primate Prefrontal Cortex Neurons , 2014, Neuron.

[120]  Andreas Nieder,et al.  Abstract rule neurons in the endbrain support intelligent behaviour in corvid songbirds , 2013, Nature Communications.

[121]  A. Phillips,et al.  A top-down perspective on dopamine, motivation and memory , 2008, Pharmacology Biochemistry and Behavior.

[122]  Anu G. Nair,et al.  Detection of phasic dopamine by D1 and D2 striatal medium spiny neurons , 2017, The Journal of physiology.

[123]  P. Dayan.  Twenty-Five Lessons from Computational Neuromodulation , 2012, Neuron.

[124]  Kuei Y Tseng,et al.  Dopamine–Glutamate Interactions Controlling Prefrontal Cortical Pyramidal Cell Excitability Involve Multiple Signaling Mechanisms , 2004, The Journal of Neuroscience.

[125]  W. Schultz,et al.  Dopamine neurons of the monkey midbrain: contingencies of responses to active touch during self-initiated arm movements. , 1990, Journal of neurophysiology.

[126]  J. Seamans,et al.  Synaptic basis of persistent activity in prefrontal cortex in vivo and in organotypic cultures. , 2003, Cerebral cortex.

[127]  J. Morrison,et al.  NMDA Receptors Subserve Persistent Neuronal Firing during Working Memory in Dorsolateral Prefrontal Cortex , 2013, Neuron.

[128]  W. Schultz.  Responses of midbrain dopamine neurons to behavioral trigger stimuli in the monkey. , 1986, Journal of neurophysiology.

[129]  D. Denys,et al.  Dopaminergic control of cognitive flexibility in humans and animals , 2013, Front. Neurosci..

[130]  E. Miller,et al.  Neural Substrates of Dopamine D2 Receptor Modulated Executive Functions in the Monkey Prefrontal Cortex. , 2015, Cerebral cortex.

[131]  P. Goldman-Rakic,et al.  Dopamine synaptic complex with pyramidal neurons in primate cerebral cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[132]  G. Shepherd,et al.  The neocortical circuit: themes and variations , 2015, Nature Neuroscience.

[133]  S. Kennerley,et al.  Heterogeneous reward signals in prefrontal cortex , 2010, Current Opinion in Neurobiology.

[134]  Andreas Nieder,et al.  Active encoding of decisions about stimulus absence in primate prefrontal cortex neurons , 2012, Proceedings of the National Academy of Sciences.

[135]  Earl K. Miller,et al.  Selective representation of relevant information by neurons in the primate prefrontal cortex , 1998, Nature.

[136]  P. Goldman-Rakic,et al.  Dopamine D2 receptor mechanisms contribute to age-related cognitive decline: the effects of quinpirole on memory and motor performance in monkeys , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[137]  Graham V. Williams,et al.  Inverted-U dopamine D1 receptor actions on prefrontal neurons engaged in working memory , 2007, Nature Neuroscience.

[138]  P. Goldman-Rakic,et al.  Distribution of dopaminergic receptors in the primate cerebral cortex: Quantitative autoradiographic analysis using [3H]raclopride, [3H]spiperone and [3H]SCH23390 , 1991, Neuroscience.

[139]  M. Carandini,et al.  Probing perceptual decisions in rodents , 2013, Nature Neuroscience.

[140]  K. C. Anderson,et al.  Single neurons in prefrontal cortex encode abstract rules , 2001, Nature.

[141]  Anne E Carpenter,et al.  Neuron-type specific signals for reward and punishment in the ventral tegmental area , 2011, Nature.

[142]  Vikaas S Sohal,et al.  Tonic or Phasic Stimulation of Dopaminergic Projections to Prefrontal Cortex Causes Mice to Maintain or Deviate from Previously Learned Behavioral Strategies , 2017, The Journal of Neuroscience.

[143]  Christos Constantinidis,et al.  A Neural Circuit Basis for Spatial Working Memory , 2004, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[144]  E. Miller,et al.  The Role of Prefrontal Dopamine D1 Receptors in the Neural Mechanisms of Associative Learning , 2012, Neuron.

[145]  E. Rolls,et al.  Computational models of schizophrenia and dopamine modulation in the prefrontal cortex , 2008, Nature Reviews Neuroscience.

[146]  T. Robbins,et al.  Impaired set-shifting and dissociable effects on tests of spatial working memory following the dopamine D2 receptor antagonist sulpiride in human volunteers , 2004, Psychopharmacology.

[147]  J. Seamans,et al.  The principal features and mechanisms of dopamine modulation in the prefrontal cortex , 2004, Progress in Neurobiology.

[148]  J. Schall,et al.  Visual and Motor Connectivity and the Distribution of Calcium-Binding Proteins in Macaque Frontal Eye Field: Implications for Saccade Target Selection , 2009, Front. Neuroanat..

[149]  O. Hikosaka,et al.  Two types of dopamine neuron distinctly convey positive and negative motivational signals , 2009, Nature.

[150]  William R. Stauffer,et al.  Dopamine prediction error responses integrate subjective value from different reward dimensions , 2014, Proceedings of the National Academy of Sciences.

[151]  P. Goldman-Rakic,et al.  D1 dopamine receptors in prefrontal cortex: involvement in working memory , 1991, Science.

[152]  P. Goldman-Rakic,et al.  Dissociation of object and spatial processing domains in primate prefrontal cortex. , 1993, Science.

[153]  W. Schultz.  Multiple dopamine functions at different time courses. , 2007, Annual review of neuroscience.

[154]  T. Robbins,et al.  Improved short-term spatial memory but impaired reversal learning following the dopamine D2 agonist bromocriptine in human volunteers , 2001, Psychopharmacology.

[155]  P. Voorn,et al.  Development of Dopamine - Containing Systems in the CNS , 1992 .

[156]  P. Goldman-Rakic,et al.  Modulation of memory fields by dopamine Dl receptors in prefrontal cortex , 1995, Nature.

[157]  A. Arnsten.  Catecholamine Influences on Dorsolateral Prefrontal Cortical Networks , 2011, Biological Psychiatry.

[158]  C. Curtis,et al.  Multiple component networks support working memory in prefrontal cortex , 2015, Proceedings of the National Academy of Sciences.

[159]  S. Kennerley,et al.  Reward-Dependent Modulation of Working Memory in Lateral Prefrontal Cortex , 2009, The Journal of Neuroscience.

[160]  J. Fuster.  Prefrontal Cortex , 2018 .

[161]  William R. Stauffer,et al.  Dopamine Neuron-Specific Optogenetic Stimulation in Rhesus Macaques , 2016, Cell.

[162]  Talia N. Lerner,et al.  Intact-Brain Analyses Reveal Distinct Information Carried by SNc Dopamine Subcircuits , 2015, Cell.

[163]  P. Goldman-Rakic,et al.  D2 receptor regulation of synaptic burst firing in prefrontal cortical pyramidal neurons. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[164]  Michael C. Anderson,et al.  Suppressing unwanted memories by executive control , 2001, Nature.

[165]  P. Goldman-Rakic,et al.  D1 Receptor in Interneurons of Macaque Prefrontal Cortex: Distribution and Subcellular Localization , 1998, The Journal of Neuroscience.

[166]  T. Moore,et al.  The role of neuromodulators in selective attention , 2011, Trends in Cognitive Sciences.

[167]  A. Nieder,et al.  Cell-type-specific modulation of targets and distractors by dopamine D1 receptors in primate prefrontal cortex , 2016, Nature Communications.

[168]  R. Romo,et al.  Neural correlate of subjective sensory experience gradually builds up across cortical areas , 2006, Proceedings of the National Academy of Sciences.

[169]  S. Floresco.  Prefrontal dopamine and behavioral flexibility: shifting from an “inverted-U” toward a family of functions , 2013, Front. Neurosci..

[170]  P. Goldman-Rakic,et al.  Localization of dopamine D4 receptors in GABAergic neurons of the primate brain , 1996, Nature.

[171]  P. Goldman-Rakic,et al.  A role for inhibition in shaping the temporal flow of information in prefrontal cortex , 2002, Nature Neuroscience.

[172]  S. Kapur,et al.  The dopamine hypothesis of schizophrenia: version III--the final common pathway. , 2009, Schizophrenia bulletin.

[173]  A. Nieder,et al.  Dopamine D2 Receptors Enhance Population Dynamics in Primate Prefrontal Working Memory Circuits , 2016, Cerebral cortex.

[174]  M. Farah,et al.  Effects of bromocriptine on human subjects depend on working memory capacity , 1997, Neuroreport.

[175]  Antonieta Lavin,et al.  Mechanisms Underlying Differential D1 versus D2 Dopamine Receptor Regulation of Inhibition in Prefrontal Cortex , 2004, The Journal of Neuroscience.

[176]  R. Silver,et al.  Shunting Inhibition Modulates Neuronal Gain during Synaptic Excitation , 2003, Neuron.

[177]  P S Goldman-Rakic,et al.  D1 dopamine receptor immunoreactivity in human and monkey cerebral cortex: predominant and extrasynaptic localization in dendritic spines. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[178]  Kelsey L. Clark,et al.  The role of prefrontal catecholamines in attention and working memory , 2014, Front. Neural Circuits.

[179]  T. Sejnowski,et al.  Neurocomputational models of working memory , 2000, Nature Neuroscience.

[180]  J. Obeso,et al.  Functional organization of the basal ganglia: Therapeutic implications for Parkinson's disease , 2008, Movement disorders : official journal of the Movement Disorder Society.

[181]  F. Sundler,et al.  Neuronal gastrin-releasing peptide in the mammalian gut and pancreas , 1983, Neuroscience.

[182]  N. Uchida,et al.  Opposite initialization to novel cues in dopamine signaling in ventral and posterior striatum in mice , 2016, eLife.

[183]  Praneeth Namburi,et al.  Dopamine enhances signal-to-noise ratio in cortical-brainstem encoding of aversive stimuli , 2018, Nature.

[184]  Nathan R. Wilson,et al.  Division and subtraction by distinct cortical inhibitory networks in vivo , 2012, Nature.

[185]  D. Johnston,et al.  Subcircuit-specific neuromodulation in the prefrontal cortex , 2014, Front. Neural Circuits.

[186]  R. Romo,et al.  Dopaminergic activity coincides with stimulus detection by the frontal lobe , 2012, Neuroscience.

[187]  P. Goldman-Rakic,et al.  Destruction and Creation of Spatial Tuning by Disinhibition: GABAA Blockade of Prefrontal Cortical Neurons Engaged by Working Memory , 2000, The Journal of Neuroscience.

[188]  T. Sejnowski,et al.  Dopamine D1/D5 receptor modulation of excitatory synaptic inputs to layer V prefrontal cortex neurons. , 2001, Proceedings of the National Academy of Sciences of the United States of America.